Thursday, September 13, 2012

Because Osedax were originally identified colonizing
cetacean skeletons, they were originally interpreted as being whale-fall
specialists. In order to test the hypothesis that Osedax are cetacean
carcass specialists, Jones et al. (2008) experimentally deployed cow bones on
the seafloor in Monterey Bay.
They attached cow bones to a PVC “tree” on the seafloor, so that the bones
would not be in contact with the sediment (with the chance of being covered in
sediment. Within a year, the bones were colonized by Osedax. As cow
skeletons are probably not typically delivered to the deep sea floor – although
given the presence of rare land mammals and dinosaurs in marine fossil assemblages,
it does happen, albeit rarely – it suggests that Osedax is not really a
cetacean specialist, and can colonize the bones of other mammals. Jones et al.
(2008) suggested that Osedax not only colonize the skeletons of baleen
whales, but also bones of dolphins, porpoises, sea lions, and seals that
reached the seafloor. They further suggested that future experiments should
include other-non cetacean bones. One could make the observation that large,
domesticated artiodactyls are not only closely related to cetaceans, but also
have fatty bones; so perhaps it’s not surprising that cow bones make
appropriate habitat for bone eating worms.

Modern cow bones implanted on a PVC "tree" on the seafloor, with closeup of Osedax worms emerging from the bone. From Jones et al. (2008).

This paper seemed to stir up some controversy, and generated
a sharp response by Glover et al. (2008) who commented on several aspects of
the study which may (or may not…) invalidate observations of cow bone
colonization. They argue that Osedax probably qualifies as a whale-fall
specialist, because whale skeletons comprise the majority of its “diet”. They
indicated that no whale fall assemblages had been identified on naturally
occurring terrestrial mammal carcasses in the deep sea. They also argued that
the placement of cow bones on a metal tree above the seafloor does not
represent a naturally occurring condition; they indicate that the small bones
of land mammals would probably be buried too quickly to be colonized by Osedax.
I’m not necessarily certain this is really evidence that Osedax wasn’t
a generalist, but the inferred rarity of terrestrial vertebrate remains on the
seafloor is probably reasonable to cite as evidence of Osedax being a
whale fall specialist. Curiously, Glover et al. (2008) make the comment that
actualistic taphonomy of large land mammals shows that they are unlikely to be
transported far by rivers. This is perhaps amusing when one recalls how many
fossils we have of land mammals and dinosaurs in marine rocks – examples from
my neck of the woods include a skull of the dome-headed chalicothere Tylocephalonyx
from the marine Astoria Formation of central Oregon,
and the type skeleton of Aletopelta from the late Cretaceous of San
Diego County (a.k.a. the “ankylosaur ass”, as affectionately referred to by
some SDSU students). Furthermore – in one of Jack Horner’s first papers, he
reviewed the dinosaur record from the late Cretaceous Bearpaw Shale of Montana,
and found that numerically more nodosaurid skeletons were known at the time
from marine rocks than from terrestrial rocks.

Vrijenhoek et al. (2008) responded to the complaints of
Glover et al. (2008) and noted the age-old adage that ‘absence of evidence is
not evidence of absence’, and is certainly an excellent point in this case: the
lack of discoveries of terrestrial mammal ‘falls’ is probably not a good
indication of their existence of not: Glover et al. argued that Osedax may not
effectively colonize land mammal bones due to their small size, and it is
important to note that the same argument can be flipped on its head – small
bones are less likely to be discovered on the seafloor by ROV’s or submersibles.
Contrary to the assertion of Glover et al. (2008) that land mammals do not
frequently travel long distances in rivers (and thus float out into the sea),
Vrijenhoek et al. (2008) report on a pelvis and several hind leg bones of a
large mammalian herbivore off the coast of New Guinea at a depth of 1500
meters, discovered by submersible. These bones were also colonized by Osedax,
interestingly. Not only does this indicate that Osedax will colonize
“naturally” occurring land mammal bones, but also that such occurrences are
‘findable’. Vrijenhoek et al. (2008) report that rice was found on the seafloor
around the bones, and they interpreted it as discarded waste from a passing
ship; furthermore, the pelvis shows a distinct butcher’s sawmark, indicating it
did not arrive naturally.

Partial hindlimbs of a terrestrial mammal found on the seafloor, complete with Osedax... and a pile of rice? This appears to represent waste chucked overboard a ship. From Vrijenhoek et al. (2008).

A beautifully sculpted model of the giant Japanese plotopterid, Copeteryx. Sculpted by Hirokazu Tokugawa (from a-fragi.blogspot.com).Oligocene bones of a close relative from Washington state- Tonsala - have been found with trace fossils identifiable as Osedax.

In late 2010, Steffen Kiel and colleagues published another
article on fossil Osedax borings – this time on early Oligocene bird
bones from the Olympic Peninsula. These were bones of the extinct bird Tonsala
hildegardae – a flightless, penguin-like plotopterid bird. Plotopterids
such as Tonsala, Copteryx, Hokkaidornis, and Plotopterum
are gigantic birds that went extinct during the Miocene; they are known from Japan,
California, Oregon,
Washington, and British
Columbia. These giant birds were up to 2 meters in
height, and represent the Northern Pacific analogs of giant Paleogene penguins
(e.g. Kairuku, Icadyptes, Platydyptes). Bones of Tonsala
were found to have numerous small Osedax pinholes, in addition to
typical Osedax borings when CT-data were examined. To recap from part 2, these boreholes are where the Osedax stalks and gills extend out from the bone; below, the borings are confluent with bioeroded galleries roofed over by thin walls of outer (cortical) bone left. Not only does this
further indicate that Osedax has naturally colonized non-cetaceans
through the course of geologic time, but also that Osedax would have had
a suitable source of bones prior to the Eocene evolution of cetaceans. This
further suggests that a Cretaceous rather than Eocene divergence date of modern
Osedax species (these are the two hypothesized divergence dates in the
literature, depending upon which calibration is used).

Fossil record of large marine birds during the latest Cretaceous and Paleogene; these birds may have bridged the gap for Osedax between the extinction of large marine reptiles and the emergence of large, oceangoing cetaceans in the middle Eocene. From Kiel et al. (2011).

The next year, Rouse et al. (2011) published a short
paper on another experiment in order to further test the whale-specialist
hypothesis. Rouse et al. experimentally deployed large fish bones in small wire
cages, and observed Osedax colonization after only 5 months. This is far
more surprising than cow bones, as fish bones have avascular histology (i.e.
dense bone without pore space), which is perhaps as far from the lipid-rich,
osteoporotic bones of cetaceans that you can get among vertebrates. This not
only lends support to the idea that Osedax may naturally colonize
non-cetaceans, but also that non-cetacean bones (such as those from birds and
bony fish) would have sustained Osedax during the Paleocene and early
Eocene, after marine reptiles went extinct but before large oceangoing
cetaceans evolved.

Fish bones experimentally deployed on the seafloor, and hosting Osedax worms, indicating they have a much taxonomically wider palette of bony substrates for colonization and consumption. From Rouse et al. (2011).

All in all, it appears as though modern Osedax probably
does occur most commonly on whale skeletons rather than other vertebrates, but
that it has colonized the remains of other vertebrate groups through time.
Unfortunately, our fossil record of Osedax boreholes is restricted to a
handful of bones from the Oligocene and Pliocene; the real test of Osedax
evolution will be in the Eocene and Late Cretaceous. On one hand, I somewhat
doubt that we will find Cretaceous Osedax borings, if they have not been
identified as of yet. On the other hand – the fact that Osedax borings
are so small, and have only been in the collective conscience of marine
vertebrate paleontologists for only a year or two, they may legitimately be
unidentified in currently established fossil collections of late Cretaceous
marine reptiles. If we don’t find late Cretaceous Osedax, it might be
reasonable to hypothesize that they arose with Eocene cetaceans, as proposed by
some biologists.

Saturday, September 8, 2012

A schematic showing a 3d model of an Osedax bone boring. (Source: University of Leeds)

After taking a taphonomy course during my undergraduate
program – roughly a year after Osedax was discovered – I had come across
several references to bone eating worms. But because only a few papers had been
published on fossil whale falls, and whale falls appear to be relatively rare
in the fossil record, I didn’t really seriously expect traces of Osedax worms
to be found in fossils. Surprisingly, I only had to wait five years. In 2010, a
number of papers were published regarding possible Osedax traces – and
what modern Osedax borings look like.

To start with – the first fossil record of whale falls was
reported not very long after the first modern whale falls were reported.
Squires et al. (1991) reported on Oligocene cetaceanspreserved with chemautotrophic mollusks,
which were closely related to mollusks already known from cold seeps.
Subsequently, a number of other fossil whale fall assemblages were reported
(Goedert et al., 1995; Amano and Little, 2005; Pyenson and Haasl, 2007).

In February 2010, some borings were reported from Miocene
baleen whale bones from Spain;
they were cylindrical, up to 5cm deep and 1-3mm across, with numerous
teardrop-shaped lobes internally. These were interpreted by the authors to
represent Osedax worm borings (Muniz et al., 2010). Furthermore, the
authors were able to name a new ichnospecies – trace fossils are given Linnean
binomial names in ichnotaxonomy, a parataxonomic system. They named the trace
fossil Trypanites ionasi; other ichnospecies of Trypanites are
borings in hard substrates.

Traces of Trypanites ionasi, from the Miocene of Spain. From Muniz et al. 2010.

A few months later, in April – Steffen Kiel, Jim Goedert,
and colleagues reported on possible Osedax traces in Oligocene cetacean
bones from the Olympic Peninsula. More importantly, they also reported on what
exactly modern Osedax borings actually look like – data which had not
yet been published in the whale fall literature yet. The borings that Kiel et
al. (2010) reported on from modern and fossil whale bones had tiny boreholes in
the cortical bone surface, and the cortical bone was bioeroded into large
coalesced galleries underneath the exterior bone surface. Where the borings
coalesced, only the outermost layer of bone was left as a thin veneer. In life,
the stalks exit the bone through the tiny boreholes, and the “roots” occupy the
bioeroded galleries. The modern and fossil traces were analyzed by CT scans,
used to construct 3d models of the borings.

Oddly enough, these borings don’t really resemble those
reported by Muniz et al. (2010) – at all. It is certainly feasible that those reported
by Muniz et al. are some other species of Osedax, and we only have a few
examples of published modern Osedax traces. However, the fact that
Oligocene and modern traces are nearly identical suggests that there is some
degree of conservatism in boring shape. So, who really knows what made the
traces in the Spanish whale bones. It’s understandable, as the authors of that
study didn’t report on what modern Osedax traces look like – a necessary
stepping stone for interpreting fossil remains. As an aside, one of the authors
of that study – Raul Esperante – is a well known young-earth creationist from
Loma Linda Univerisity in southern California
who has published a series of articles on whale taphonomy.

Finally, examples of Osedax traces from a modern bone: from Higgs et al. (2010).

More examples of modern Osedax traces, from Higgs et al. (2011).

More work on modern Osedax traces was published by
Higgs et al. (2010). They also used CT scans to construct 3d models of the
borings, and reported borings that were roughly similar to that reported by
Kiel et al. (2010). Higgs et al. (2010) further found that the borings were
mostly restricted to dense cortical bone, generally avoiding lipid-rich
cancellous zones. Apparently some isotopic evidence suggests that Osedax synthesizes
collagen rather than lipids, although other studies have documented Osedax in
Japanese waters that subsist on blubber and spermaceti (Higgs et al. 2010 –
references therein).

The (awesome) t-shirt Nick Higgs wore to SVP in 2009. The few marine vertebrate taphonomists at SVP - myself included - found this guy pretty damn quick.

I met Nick Higgs at the 2009 SVP meeting in Bristol, UK – I
was chatting with my friend and colleague Laura Vietti (Macalester
College/University of Michigan), who is also focused on marine vertebrate
taphonomy – and this British guy about our age came up to us, literally wearing
a T-shirt he had made which said “bone eating worms” with a picture of Osedax
infested whale bone on the back, and text saying “Lets talk: whale
taphonomy!” Needless to say, he found Laura and myself really darn quick. Nick
has subsequently invited us both to co-write a review paper on marine
vertebrate taphonomy, which is an exciting opportunity to say the least.

A beaked whale radius from the Pliocene of Tuscany, Italy, with numerous Osedax traces and pockmarks. From Higgs et al. (2011).

More recently, Nick Higgs and colleagues (2011) published
another paper on early Pliocene Osedax borings in a beaked whale radius
from Italy.
This fossil exhibited a number of different types of borings, which were
interpreted as different stages of borings. Some borings in CT-scans were well
defined, with small apertures as in Kiel et al. (2010) and Higgs et al. (2010).
Other pits had a small bit of bone caved in around the aperture (collapsed
stage), while other pits retained no overhanging bone (open-pit stage); the
last type has been eroded to the point where it looks like a crater (pockmark
stage). Some pits had coalesced, forming combined pits. Higgs et al. (2011)
also named a new ichnotaxon for these Osedax borings: Osspecus tuscia.

Two modern cetacean bones bored by Osedax. What's the significance of this figure from Higgs et al. (2011)? Stick around for part 4.

Although borings of Osedax have now been documented
from the fossil record, what exactly does it mean for taphonomy? And what does
it mean about the evolution and earliest record of Osedax? Tune in for
parts 3 and 4.

Thursday, September 6, 2012

How do we interpret the preservation of fossil marine vertebrates, like this Dorudon atrox skeleton from the Eocene of Egypt? (From Peters et al., 2011)

Unless you've lived in a cave for the last two decades or
hate science and the oceans (or all of the above), you've probably heard about
whale falls. Whale falls are one of the more fascinating aspects of modern
marine biologic research. They were only discovered relatively recently (late
1990's) and research conducted by submersible and ROV
has uncovered an amazing fauna that quickly develops around sunken whale
carcasses. Biomass is present in relatively small amounts on the seafloor, and
much of the food for critters on the abyssal plain rains down from the more
densely populated upper part of the water column. When whales die – and sink –
most of the time their carcasses will sink down to the seafloor. But whales
aren't very common, and although whales die every day – the introduction of a
whale carcass to the seafloor, from the vantage point of a seafloor organism –
is not an everyday affair. Seafloor ecology is mediated by the introduction of food,
and whale carcasses represent the most locally concentrated pulse of food in
the deep sea.

Whale vertebrae and a hagfish at a whale fall. From www.mbari.org

As a paleontologist, much of the hullabaloo about whale
falls is only of cursory interest; many of the ecological details – species
diversity at whale falls, similarity to vent and cold seep fauna, interactions
between invertebrates – are not really of much practical interest to a
vertebrate paleontologist like myself. Certainly these other issues are totally
fascinating – but I'm really only going to talk on here about the stuff that
interests me as a paleontologist, as you can easily get the perspective of a
biologist or ecologist elsewhere on the web.

Photograph of a whale fall hosting a large number of bone-eating worms (Osedax).

So why am I so interested in whale falls? Whale fall
research has generated some seriously intriguing information regarding the
taphonomy of marine mammals (cetaceans in particular; see Allison et al., 1991). Admittedly, not all
vertebrate paleontologists (marine mammal researchers included) are not
terribly interested in taphonomy. Taphonomy is the science of fossil
preservation, and is often summed up as attempting to discover everything that
happened to a fossil from "death until burial" (and sometimes, after
burial: diagenesis). This is a serious problem, as any paleontologists who hope
to do field-based research need a strong (or even mediocre) background in
taphonomy. I find taphonomy to be, on one hand – relatively intuitive, and on
the other hand – more intellectually stimulating than bread and butter
phylogenetics (this is not a slam against cladistics; I just find taphonomic problems
more interesting and challenging).

A painting of a whale fall assemblage. From www.mbari.org

Taphonomy is also very important if a paleontologist is
interested in anything relating to paleoecology: with respect to a fossil,
paleoecologic information can generally be preserved intrinsically (functional
anatomy, oxygen/carbon isotopes, etc.) or extrinsically (gut residues,
coprolites, feeding traces, juvenile/adult or other social associations, etc.).
The former category is more or less decoupled from taphonomy, as it generally
pertains to information not affected by taphonomic loss. However, once a
paleontologist wants to start talking about the nature of a fossil assemblage,
and whether it represents a mass death assemblage, a nesting ground, or
evidence of feeding behavior, these issues extend outside the bones themselves,
so to speak, and into tangential issues affected by processes of preservation.
To say anything regarding paleoecology and using extrinsic information, a
paleontologist had better do his or her damned homework; there are plenty of
examples in the published literature of non-taphonomists saying some pretty
silly things.

Because I study fossil marine mammals, whale falls provide a
wealth of data regarding what happens to a whale after it dies on the seafloor.
So, what does happen? To sum it up, in a way – a multitude of organisms rush in
to eat it. Whale fall faunas appear to show a series of successive stages
(Smith and Baco 2003):

3) Sulphophilic stage: a trophically complex assemblage of
nearly 200 species of invertebrates and microorganisms inhabit the skeleton
while lipids in the bones undergo anaerobic breakdown and emit sulphides.

A fourth stage – the reef stage – has been hypothesized for
late-stage whale falls (Smith, 2006) that are chemically inert, so to speak – and colonized
by sessile invertebrates taking advantage of higher elevation (and thus
currents) above the seafloor. However, no evidence for this stage currently exists
and it is purely hypothetical.

A group of Osedax stalks and gills growing in a whale bone.From www.mbari.org

In particular, modern whale falls have benefited
taphonomists by providing valuable information regarding rates of scavenging
and the timing of skeletonization (exposure of bones in a carcass) as well as
rates of bone degradation, burial, and the types of organisms that may leave a
physical trace record of their colonization. In 2004, a new type of whale fall
specialist was discovered infesting the bones of a baleen whale skeleton off
the coast of California: a
bone-eating “zombie” polychaete worm, named Osedax (Rouse et al., 2004). It was discovered in
massive amounts on bones, with reddish gills mounted on stalks emanating from
small holes in the bone. Roots of the worm extend into the bone, and host
symbiotic bacteria to synthesize nutrients from the bone. It is currently
debated exactly what Osedax feeds upon: lipids in the bone, or collagen.
Since 2004, a number of species of Osedax have been discovered, and are
now known worldwide from deep marine whale falls. If this parade of weirdness
wasn’t enough, the males are dwarfs, never leave the larval stage, and live
on/in the females.

An individual Osedax worm separated from its bony home. From www.mbari.org

In the next few posts, I’ll cover several issues, including
the discovery of Osedax traces in fossil bone (part 2), Osedax colonization/consumption
of other types of vertebrates (part 3), and implications for taphonomy and
possible “megabias” in the fossil record (part 4).

I highly recommend watching this video: it's not educational, per se, but if you're familiar with whale falls, it is delightfully animated. Whale Fall (afterlife of a whale).

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About the Coastal Paleontologist

I'm a paleontologist and adjunct faculty at College of Charleston in South Carolina, with research interests in Cenozoic marine vertebrates with an emphasis on marine mammals (whales, dolphins, pinnipeds, otters, sea cows, and others), but I willingly entertain brief distractions into the worlds of marine birds, sharks, and fish. My M.S. (2011, MSU-Bozeman) focused on marine vertebrate taphonomy whilst my Ph.D. (2015, U. Otago, NZ) focused on Oligocene baleen whales from New Zealand. Current research is concerned with fossil cetaceans from South Carolina including Oligocene eomysticetids, toothed mysticetes, and archaic dolphins.